Clinical Practice How Common is Halitosis?

Clinical Practice How Common is Halitosis?

Halitosis is defined an unpleasant odor of the breath, also referred to as oral malodor or simply bad breath. For an estimated 80% to 90% of individuals, halitosis is of oral origin.1Porter SR, Scully C. Oral malodour (halitosis). Br Med J 2006;333:632-5.^,2Settineri S, Mento C, Gugliotta SC, Saitta A, Terranova A, Trimarchi G, Mallamace D. Self-reported halitosis and emotional state: impact on oral conditions and treatments. Health Qual Life Outcomes 2010;8:34. Poor oral hygiene, tongue coating, periodontitis, dental caries and dry mouth are associated with halitosis.3De Boever EH, De Uzeda M, Loesche WJ. Relationship between volatile sulfur compounds, BANA-hydrolyzing bacteria and gingival health in patients with and without complaints of oral malodor. J Clin Dent 1994;4(4):114-9.^,4Kleinberg I, Wolff MS, Codipilly DM. ADA Role of saliva in oral dryness, oral feel and oral malodour. Int Dent J 2002;52 (Suppl 3):236‑40.^,5American Dental Association. Bad breath. Causes and tips for controlling it. J Am Dent Assoc 2012;143(9):1053.6Quirynen M, Dadamio J, Van den Velde S, De Smit M, Dekeyser C, Van Tornout M and Vanderkerckhove B. Characteristics of 2000 patients who visited a halitosis clinic. J Clin Periodontol 2009;36:970–5. Accumulated oral biofilm and sloughed epithelial cells on surfaces result in bacterial activity that produces malodorous volatile sulfur compounds (VSCs), short-chain fatty acids and diamines.7De Geest S, Laleman I, Teughels W, Dekeyser C, Quirynen M. Periodontal diseases as a source of halitosis: a review of the evidence and treatment approaches for dentists and dental hygienists. Periodontol 2016;71:213-27.^,8Scully C, Felix DH. Oral medicine – update for the dental practitioner: Oral malodour. Br Dent J 2005;199:498‑500. (Table 1) In one large study of 2,000 patients,6Quirynen M, Dadamio J, Van den Velde S, De Smit M, Dekeyser C, Van Tornout M and Vanderkerckhove B. Characteristics of 2000 patients who visited a halitosis clinic. J Clin Periodontol 2009;36:970–5. tongue coating and/or periodontal disease were responsible for 76% of cases of halitosis of oral origin, and in another study tongue coating was strongly associated with self-perceived halitosis.6Quirynen M, Dadamio J, Van den Velde S, De Smit M, Dekeyser C, Van Tornout M and Vanderkerckhove B. Characteristics of 2000 patients who visited a halitosis clinic. J Clin Periodontol 2009;36:970–5.^,9Youngnak-Piboonratanakit P, Vachirarojpisan T. Prevalence of self-perceived oral malodor in a group of Thai dental patients. J Dent (Tehran) 2010;7(4):196–204.

Halitosis of non-oral origin is associated with disorders and infections of the nose and sinuses, throat and the gastrointestinal tract.1Porter SR, Scully C. Oral malodour (halitosis). Br Med J 2006;333:632-5.^,10Hughes FJ, McNab R. Oral malodour–a review. Arch Oral Biol 2008;53 (Suppl 1):S1-7. Examples include adenoid hypertrophy which in one study resulted in 22% of children experiencing chronic halitosis, and an association has been found for the severity of gastroesophageal reflux disease and the severity of self-reported halitosis.11Sikorska-Zuk M, Bochnia M. Halitosis in children with adenoid hypertrophy. J Breath Res 2018;12(2):026011.^,12Struch F, Schwahn C, Wallaschofski H, Grabe HJ, Volzke H, Lerch MM, Meisel P, Kocher T. Self-reported halitosis and gastro-esophageal reflux disease in the general population. J Gen Intern Med 2008;23(3):260-6. Other less common, non-oral causes include end-stage renal disease, hepatic failure, diabetic ketoacidosis, and certain medications.1Porter SR, Scully C. Oral malodour (halitosis). Br Med J 2006;333:632-5.^,10Hughes FJ, McNab R. Oral malodour–a review. Arch Oral Biol 2008;53 (Suppl 1):S1-7.

Non-oral causes of halitosis must be considered in the differential diagnosis. It is also important to recognize that some patient reports of halitosis have a psychological basis, rather than being the result of a disease or disorder of an anatomical structure. One important question is the true prevalence of halitosis, as this condition is an important issue for the general population.

Classification of Halitosis

Patients self-reporting halitosis may have transient halitosis, pseudohalitosis, chronic (true) halitosis or halitophobia.1Porter SR, Scully C. Oral malodour (halitosis). Br Med J 2006;333:632-5.^,8Scully C, Felix DH. Oral medicine – update for the dental practitioner: Oral malodour. Br Dent J 2005;199:498‑500. Causes of transient halitosis include mouthbreathing at night, ingestion of alcohol or odiferous foods such as garlic, tobacco use, temporary conditions such as dry socket, and short-term medication use.8Scully C, Felix DH. Oral medicine – update for the dental practitioner: Oral malodour. Br Dent J 2005;199:498‑500. Pseudohalitosis occurs when a patient repeatedly complains of halitosis that is not perceived by others and cannot be confirmed using organoleptic testing or by measuring VSC levels.13Yaegaki K, Coil JM. Examination, classification, and treatment of halitosis; clinical perspectives. J Can Dent Assoc 2000;66(5):257-61.^,14Seemann R, Conceicao MD, Filippi A, Greenman J, Lenton P, Nachnani S, Quirynen M, Roldan S, Schulze H, Sterer N, Tangerman A, Winkel EG, Yaegaki K, Rosenberg M. Halitosis management by the general dental practitioner—results of an international consensus workshop. J Breath Res 2014;8:017101. Conversely, chronic halitosis is malodor that is perceived by others, at a socially unacceptable level, and that can be confirmed by testing.13Yaegaki K, Coil JM. Examination, classification, and treatment of halitosis; clinical perspectives. J Can Dent Assoc 2000;66(5):257-61.^,14Seemann R, Conceicao MD, Filippi A, Greenman J, Lenton P, Nachnani S, Quirynen M, Roldan S, Schulze H, Sterer N, Tangerman A, Winkel EG, Yaegaki K, Rosenberg M. Halitosis management by the general dental practitioner—results of an international consensus workshop. J Breath Res 2014;8:017101. Patients with halitophobia fear that they have halitosis, and these patients may require referral to a mental health professional for evaluation and support.15Soder B, Johansson B, Soder PO. The relation between foetor ex ore, oral hygiene and periodontal disease. Swed Dent J 2000;24:73-82.

Prevalence of halitosis

Estimates for the prevalence of halitosis range widely.16Hammad MM, Darwazeh AM, Al-Waeli H, Tarakji B, Alhadithy TT. Prevalence and awareness of halitosis in a sample of Jordanian population. J Int Soc Prev Commun Dent 2014;4:S178-86.^,17Rösing CK, Loesche W. Halitosis: an overview of epidemiology, etiology and clinical management. Braz Oral Res 2011;25(5):466-71. It has also been found that some patients with chronic halitosis may underestimate their condition and/or not complain.18Bornstein MM, Kislig K, Hoti BB, Seemann R, Lussi A. Prevalence of halitosis in the population of the city of Bern, Switzerland: A study comparing clinical and self-reported data. Eur J Oral Sci 2009;117:261-7. A recent systematic review and meta-analysis of 13 population-based studies, with almost 400,000 participants in total, was the first to further examine halitosis from a global perspective.19Silva MF, Leite FRM, Ferreira LB, Pola NM, Scannapieco FA, Demarco FF, Nascimento GG. Estimated prevalence of halitosis: a systematic review and meta-regression analysis. Clin Oral Investig 2018;22(1):47-55. The overall prevalence of halitosis was found to be 31.8%, ranging from 2.4% to 55%. While significant study heterogeneity was present, 60% of the differences in prevalence were due to socioeconomic status and when the study was conducted. A prevalence of almost 40% was found for low-to-middle income countries compared with 29% for high-income countries, believed to be associated with the great burden of oral disease experienced in poorer countries. (Figure 1) In addition, prevalences of 33.9%, 30.7% and 28% were found for self-reported halitosis, organoleptic assessment and VSC measurements, respectively.19Silva MF, Leite FRM, Ferreira LB, Pola NM, Scannapieco FA, Demarco FF, Nascimento GG. Estimated prevalence of halitosis: a systematic review and meta-regression analysis. Clin Oral Investig 2018;22(1):47-55. In contrast, an earlier study found a weak association between self-reported halitosis and objective assessment.18Bornstein MM, Kislig K, Hoti BB, Seemann R, Lussi A. Prevalence of halitosis in the population of the city of Bern, Switzerland: A study comparing clinical and self-reported data. Eur J Oral Sci 2009;117:261-7.

Figure 1.
Prevalence of halitosis in low to moderate- and high-income countries

Influence of gender and age on prevalence

Studies differ regarding gender and age differences and the prevalence of halitosis. In one study, 66% of women self-perceived their halitosis to be worse than indicated by organoleptic scoring, compared to 48% of men. It was concluded that the perception by the male subjects was more objective.20Romano F, Pigella E, Guzzi N, Aimetti M. Patients’ self-assessment of oral malodour and its relationship with organoleptic scores and oral conditions. Int J Dent Hyg 2010;8(1):41-6. A higher reported prevalence among females has been reported by others.2Settineri S, Mento C, Gugliotta SC, Saitta A, Terranova A, Trimarchi G, Mallamace D. Self-reported halitosis and emotional state: impact on oral conditions and treatments. Health Qual Life Outcomes 2010;8:34. In contrast, in a survey of more than 1500 individuals in Kuwait, 23% of participants self-reported halitosis, with similar prevalences for males and females.21Al-Ansari JM, Boodai H, Al-Sumait N, Al-Khabbaz AK, Al-Shammari KF, Salako N. Factors associated with self-reported halitosis in Kuwaiti patients. J Dent 2006;34(7):444-9. Other studies reported a higher prevalence in males. In a Brazilian survey of university students, while the prevalence of persistent halitosis within households was low, males had a three-fold likelihood of reporting halitosis than females.22Nadanovsky P, Carvalho LB, Ponce de Leon A. Oral malodour and its association with age and sex in a general population in Brazil. Oral Dis 2007;13(1):105-9.^,23Almas K, Al-Hawish A, Al-Khamis W. Oral hygiene practices, smoking habit, and self-perceived oral malodor among dental students. J Contemp Dent Pract 2003;4(4):77-90. Further, similar prevalences for males and females have been found in other studies.9Youngnak-Piboonratanakit P, Vachirarojpisan T. Prevalence of self-perceived oral malodor in a group of Thai dental patients. J Dent (Tehran) 2010;7(4):196–204.^,24Nalcaci R, Baran I. Factors associated with self-reported halitosis (SRH) and perceived taste disturbance (PTD) in elderly. Arch Gerontol Geriatr 2008;46(3):307-16. In addition, self-perceived halitosis has been found to be higher for individuals over 30 years-of-age.9Youngnak-Piboonratanakit P, Vachirarojpisan T. Prevalence of self-perceived oral malodor in a group of Thai dental patients. J Dent (Tehran) 2010;7(4):196–204. Additionally, approximately 75% of elderly complaining of halitosis suffered from dry mouth, which is an important risk factor for halitosis.

Initial awareness of halitosis

It is well-recognized that individuals with halitosis may not perceive that they have halitosis and first learn of it from another person.2Settineri S, Mento C, Gugliotta SC, Saitta A, Terranova A, Trimarchi G, Mallamace D. Self-reported halitosis and emotional state: impact on oral conditions and treatments. Health Qual Life Outcomes 2010;8:34.^,25de Jongh A, van Wijk AK, Horstman M, de Baat C. Self-perceived halitosis influences social interactions. BMC Oral Health 2016;16:31. In a survey of almost 400 female university students (18 to 35 years-of-age) in Saudi Arabia, only 21% reported that they had halitosis while 78% reported having identified other individuals with this condition.26Bin Mubayrik A, Al Hamdan R, Al Hadlaq EM, AlBagieh H, AlAhmed D, Jaddoh H, Demyati M, Shryei RA. Self-perception, knowledge, and awareness of halitosis among female university students. Clin Cosmet Investig Dent 2017;9:45-52. One of the conclusions was that participants had low levels of self-perception of halitosis. In addition, more than four-fifths of respondents stated that they would not alert a colleague or friend who had halitosis. In a Japanese study, 24% of individuals with halitosis reported first noticing it themselves.27Zaitsu T, Ueno M, Shinada K, Wright FA, Kawaguchi Y. Social anxiety disorder in genuine halitosis patients. Health Qual Life Outcomes 2011;9:94. Forty-six percent and 67%, respectively, had been told they had halitosis by other people or/and suspected it based on the reaction of others. (Figure 2) In another study with more than 1,000 participants, anxiety related to the dentist-patient relationship was one of the factors most associated with self-perceived halitosis.2Struch F, Schwahn C, Wallaschofski H, Grabe HJ, Volzke H, Lerch MM, Meisel P, Kocher T. Self-reported halitosis and gastro-esophageal reflux disease in the general population. J Gen Intern Med 2008;23(3):260-6.

Figure 2.
Source of initial awareness of halitosis

The importance of halitosis

Halitosis impacts social functioning, psychological well-being and overall quality of life.2Struch F, Schwahn C, Wallaschofski H, Grabe HJ, Volzke H, Lerch MM, Meisel P, Kocher T. Self-reported halitosis and gastro-esophageal reflux disease in the general population. J Gen Intern Med 2008;23(3):260-6.^,22Nadanovsky P, Carvalho LB, Ponce de Leon A. Oral malodour and its association with age and sex in a general population in Brazil. Oral Dis 2007;13(1):105-9.^,27Zaitsu T, Ueno M, Shinada K, Wright FA, Kawaguchi Y. Social anxiety disorder in genuine halitosis patients. Health Qual Life Outcomes 2011;9:94.^,28Lu HX, Chen XL, Wong M, Zhu C, Ye W. Oral health impact of halitosis in Chinese adults. Int J Dent Hyg 2016.^,29Troger B, Laranjeira de Almeida Jr H, Duquia RP. Emotional impact of halitosis. Trends Psych Psychother 2014;36(4):Porto Alegre. Among young adult male participants who complained of halitosis in one study, 70% felt ashamed, 38% depressed and 38% tense.29Troger B, Laranjeira de Almeida Jr H, Duquia RP. Emotional impact of halitosis. Trends Psych Psychother 2014;36(4):Porto Alegre. These individuals also reported significant difficulty with social interactions, and 72%, 31%, 30% and 26%, respectively, were not comfortable having conversations, avoided smiling, reported dating difficulties and also avoided social interactions. (Figure 3) These findings are supported by other reports in which halitosis was reported to impact social interactions and psychological well-being.2Struch F, Schwahn C, Wallaschofski H, Grabe HJ, Volzke H, Lerch MM, Meisel P, Kocher T. Self-reported halitosis and gastro-esophageal reflux disease in the general population. J Gen Intern Med 2008;23(3):260-6.^,22Nadanovsky P, Carvalho LB, Ponce de Leon A. Oral malodour and its association with age and sex in a general population in Brazil. Oral Dis 2007;13(1):105-9.^,26Bin Mubayrik A, Al Hamdan R, Al Hadlaq EM, AlBagieh H, AlAhmed D, Jaddoh H, Demyati M, Shryei RA. Self-perception, knowledge, and awareness of halitosis among female university students. Clin Cosmet Investig Dent 2017;9:45-52.

Figure 3. Emotions and difficulties experienced by individuals with halitosis

A Dutch study provides a further example of impaired social interaction. In the two groups within the study, 65% and 71%, respectively, reported that they thought about their oral (mal)odor sometimes/often/always when first meeting individuals and kept a distance from individuals. This was more likely the more severe they perceived their oral malodor to be.25de Jongh A, van Wijk AK, Horstman M, de Baat C. Self-perceived halitosis influences social interactions. BMC Oral Health 2016;16:31. In another study, it was found that the psychological well-being of patients correlated with all measures in the psychological assessment tool with the severity of chronic halitosis.30Suzuki N, Yoneda M, Naito T, Iwamoto T, Hirofuji T. Relationship between halitosis and psychologic status. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;106(4):542-7. This correlation was not observed in patients with pseudohalitosis. However, a study evaluating the relationship of psychological traits and subjective halitosis found that conditions such as anxiety and depression were associated with subjective halitosis.31Vali A, Roohafza H, Keshteli AH, Afghari P, Javad Shirani M, Afshar H, Savabi O, Adibi P. Relationship between subjective halitosis and psychological factors. Int Dent J 2015;65(3):120-6.

Conclusions

Halitosis is an important personal problem, affecting social interactions and the overall well-being of patients. While some patients self-perceive/self-report halitosis and ask about treatment, others do not. Questions on halitosis should be a component of patient evaluations followed by management of halitosis as indicated. In addition, when halitosis of oral origin is ruled out, or when pseudohalitosis or halitophobia is suspected, patients should be referred to a medical provider/specialist for further evaluation and support.

Given the prevalence of halitosis, understanding the basis for this condition and its impact on individuals is critical. Treatment of halitosis requires patient education and professional care, not only by dental professionals, but may also require psychological support as it is a problem that leads to avoidance behaviors and thereby limits relationships. With aging populations, and the increased incidence of chronic diseases, management of persons with halitosis will likely become of greater importance in clinical dental practice.

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